Human gut Bacteroidetes can utilize yeast mannan through a selfish mechanism

Fiona Cuskin, Elisabeth C. Lowe, Max J. Temple, Yanping Zhu, Elizabeth A. Cameron, Nicholas A. Pudlo, Nathan T. Porter, Karthik Urs, Andrew J. Thompson, Alan Cartmell, Artur Rogowski, Brian S. Hamilton, Rui Chen, Thomas J. Tolbert, Kathleen Piens, Debby Bracke, Wouter Vervecken, Zalihe Hakki, Gaetano Speciale, Jose L. Munōz-Munōz, Andrew Day, Maria J. Peña, Richard McLean, Michael D. Suits, Alisdair B. Boraston, Todd Atherly, Cherie J. Ziemer, Spencer J. Williams, Gideon J. Davies, D. Wade Abbott (), Eric C. Martens () and Harry J. Gilbert ()
Additional contact information
Fiona Cuskin: Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle-upon-Tyne NE2 4HH, UK
Elisabeth C. Lowe: Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle-upon-Tyne NE2 4HH, UK
Max J. Temple: Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle-upon-Tyne NE2 4HH, UK
Yanping Zhu: Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle-upon-Tyne NE2 4HH, UK
Elizabeth A. Cameron: University of Michigan Medical School
Nicholas A. Pudlo: University of Michigan Medical School
Nathan T. Porter: University of Michigan Medical School
Karthik Urs: University of Michigan Medical School
Andrew J. Thompson: University of York, York YO10 5DD, UK
Alan Cartmell: School of Chemistry and Bio21 Molecular Science and Biotechnology Institute, University of Melbourne
Artur Rogowski: Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle-upon-Tyne NE2 4HH, UK
Brian S. Hamilton: Interdisciplinary Biochemistry Graduate Program, Indiana University, 800 E. Kirkwood Avenue, Bloomington, Indiana 47405, USA
Rui Chen: Indiana University, 800 E. Kirkwood Avenue, Bloomington, Indiana 47405, USA
Thomas J. Tolbert: University of Kansas School of Pharmacy, 2095 Constant Avenue, Lawrence, Kansas 66047, USA
Kathleen Piens: Oxyrane, 9052 Ghent, Belgium
Debby Bracke: Oxyrane, 9052 Ghent, Belgium
Wouter Vervecken: Oxyrane, 9052 Ghent, Belgium
Zalihe Hakki: School of Chemistry and Bio21 Molecular Science and Biotechnology Institute, University of Melbourne
Gaetano Speciale: School of Chemistry and Bio21 Molecular Science and Biotechnology Institute, University of Melbourne
Jose L. Munōz-Munōz: Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle-upon-Tyne NE2 4HH, UK
Andrew Day: Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle-upon-Tyne NE2 4HH, UK
Maria J. Peña: Complex Carbohydrate Research Center, The University of Georgia, 315 Riverbend Road, Athens, Georgia 30602, USA
Richard McLean: Agriculture and Agri-Food Canada, Lethbridge Research Centre, Lethbridge, Alberta T1J 4B1, Canada
Michael D. Suits: Biochemistry and Microbiology, University of Victoria, Victoria, British Columbia V8P 5C2, Canada
Alisdair B. Boraston: Biochemistry and Microbiology, University of Victoria, Victoria, British Columbia V8P 5C2, Canada
Todd Atherly: USDA, Agricultural Research Service, National Laboratory for Agriculture and the Environment, Ames, Iowa 50011, USA
Cherie J. Ziemer: USDA, Agricultural Research Service, National Laboratory for Agriculture and the Environment, Ames, Iowa 50011, USA
Spencer J. Williams: School of Chemistry and Bio21 Molecular Science and Biotechnology Institute, University of Melbourne
Gideon J. Davies: University of York, York YO10 5DD, UK
D. Wade Abbott: Complex Carbohydrate Research Center, The University of Georgia, 315 Riverbend Road, Athens, Georgia 30602, USA
Eric C. Martens: University of Michigan Medical School
Harry J. Gilbert: Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle-upon-Tyne NE2 4HH, UK

Nature, 2015, vol. 517, issue 7533, 165-169

Abstract: Abstract Yeasts, which have been a component of the human diet for at least 7,000 years, possess an elaborate cell wall α-mannan. The influence of yeast mannan on the ecology of the human microbiota is unknown. Here we show that yeast α-mannan is a viable food source for the Gram-negative bacterium Bacteroides thetaiotaomicron, a dominant member of the microbiota. Detailed biochemical analysis and targeted gene disruption studies support a model whereby limited cleavage of α-mannan on the surface generates large oligosaccharides that are subsequently depolymerized to mannose by the action of periplasmic enzymes. Co-culturing studies showed that metabolism of yeast mannan by B. thetaiotaomicron presents a ‘selfish’ model for the catabolism of this difficult to breakdown polysaccharide. Genomic comparison with B. thetaiotaomicron in conjunction with cell culture studies show that a cohort of highly successful members of the microbiota has evolved to consume sterically-restricted yeast glycans, an adaptation that may reflect the incorporation of eukaryotic microorganisms into the human diet.

Date: 2015
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DOI: 10.1038/nature13995

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